Dissociation of sad facial expressions and autonomic

nervous system responding in boys with disruptive

behavior disorders

PENNY MARSH, THEODORE P. BEAUCHAINE, and BAILEY WILLIAMSDepartment of Psychology, University of Washington, Seattle, Washington, USA

Abstract

Although deficiencies in emotional responding have been linked to externalizing behaviors in children, little is known

about how discrete response systems (e.g., expressive, physiological) are coordinated during emotional challenge

among these youth. We examined time-linked correspondence of sad facial expressions and autonomic reactivity

during an empathy-eliciting task among boys with disruptive behavior disorders (n5 31) and controls (n5 23). For

controls, sad facial expressions were associated with reduced sympathetic (lower skin conductance level, lengthened

cardiac preejection period [PEP]) and increased parasympathetic (higher respiratory sinus arrhythmia [RSA]) activity.

In contrast, no correspondence between facial expressions and autonomic reactivity was observed among boys with

conduct problems. Furthermore, low correspondence between facial expressions and PEP predicted externalizing

symptom severity, whereas low correspondence between facial expressions and RSA predicted internalizing symptom

severity.

Descriptors: Conduct problems, Disruptive behavior, Facial expression, Sadness, Autonomic reactivity

Conduct disorder (CD) and oppositional defiant disorder

(ODD), jointly labeled as disruptive behavior disorders (DBDs)

in the DSM-IV-TR (American Psychiatric Association, 2000),

are among the most common mental health problems facing

youth (Achenbach & Howell, 1993; Knitzer, Steinberg, &

Fleisch, 1991). There is now a growing body of literature sug-

gesting that children and adolescents withDBDs have difficulties

with several domains of empathic responding, including emo-

tional processing and self-appraisals of emotional experiences

(deWied, Goudena, &Matthys, 2005; Douglas & Strayer, 1996;

Herpertz et al., 2005; Strand & Nowicki, 1999). However, other

components of empathic responding such as displays of sad facial

expressions and autonomic reactivity have only begun to receive

empirical attention (Blair, 1999; de Wied et al., 2005; Douglas &

Strayer, 1996; Herpertz et al., 2005).

Functionalist theories of emotion suggests that the synchro-

nization of emotional response systems plays a critical role in

emotional health and that desynchronization contributes to the

emergence and maintenance of psychopathology (see Ekman,

1992; Kring, Kerr, Smith, & Neale, 1993; Levenson, 1994; Ma-

uss, Levenson, McCarter, Wilhelm, & Gross, 2005; Sloan,

Strauss, Quirk, & Sajatovic, 1997). According to this perspective,

as emotions unfold over time, the coordination of emotional

appraisal, expressive behavior, and physiological responses

should improve the reliability and precision of emotion cues

and promote efficient behavioral and social responses (Levenson,

1994). To date, empirical support for this hypothesis has been

mixed (Feldman-Barrett, 2006), with some authors finding low

to moderate correlations between experiential, behavioral, and

physiological response domains (Buck, 1977; Gross & Levenson,

1993, 1997; Kettunen, Ravaja, Naatanen, Keltikangas-Jarvinen,

2000; Lanzetta, Cartwright-Smith, & Kleck, 1976; Mauss et al.,

2005), others reporting discrepancies in the direction of effects

(Notarius & Levenson, 1979), and still others reporting no re-

lationship at all (Mauss, Wilhelm, & Gross, 2004).

Recently, several researchers have suggested that inconsistent

findings may be the result of methodological limitations in prior

research (for a review, see Mauss et al., 2005). For example,

within-participant designs assessing correlations between facial

sadness and physiology for an individual over time may be more

sensitive and more relevant to questions of response coherence

than more commonly used between-participants designs that as-

sess whether people who tend to show more facial sadness also

have stronger physiological responses.

In addition, few of the studies conducted to date in which

response coherence has been examined have included differen-

tiatedmeasures of autonomic nervous system (ANS) responding.

Yet empirical work has demonstrated that parasympathetic

(PNS) and sympathetic (SNS) nervous system influences on

This study was supported by grants from the National Science Foun-

dation (GRFPDGE0203031) to PennyMarsh and theNational Institute

of Mental Health (R01 MH63699) to Theodore P. Beauchaine.Address reprint requests to: Theodore P. Beauchaine, Department of

Psychology, University of Washington, Box 351525, Seattle, WA 98195-1525, USA. E-mail: tbeaucha@u.washington.edu

Psychophysiology, 45 (2008), 100–110. Blackwell Publishing Inc. Printed in the USA.Copyright r 2007 Society for Psychophysiological ResearchDOI: 10.1111/j.1469-8986.2007.00603.x

100

heart rate often operate with considerable independence in

affecting cardiac chronotropy (Berntson, Cacioppo, Quigley, &

Fabro, 1994; Cacioppo, Uchino, & Berntson, 1994). This sug-

gests that studies of response coherence that include measures of

physiological responding may benefit from using independent

indicators of PNS (respiratory sinus arrhythmia) and SNS

(electrodermal responding, cardiac preejection period) activation

rather than using measures that are influenced concurrently by

both autonomic branches (heart rate). For example, response

coherence between electrodermal responding (EDR) and facial

affect assessed using a within-participant design during episodes

of sadness is moderate to high in samples of healthy adults

(Mauss et al., 2005).

Preliminary research suggests that there are marked individ-

ual differences in the degree of response coherence and that defi-

cits in emotion regulation capabilities and/or attempts to control

emotional expressionmay cause uncoupling of response domains

for some individuals (Mauss et al., 2005). Along these lines, dis-

sociation of emotion response systems has been noted in those

with depression and schizophrenia, two disorders that are char-

acterized by dysregulated emotion, and among individuals low in

dispositional emotion expressivity (Gross, John, & Richards,

2000; Kring et al., 1993; Sloan et al., 1997). Yet surprisingly, no

research has explored the extent to which youth with DBDs may

exhibit less correspondence across emotional response systems

(e.g., facial expression, autonomic reactivity) than their typically

developing peers. In this article, time-linked correspondence be-

tween facial expressions of sadness and autonomic responding

during a sad emotion induction are compared between boys with

DBDs and typically developing controls.

Until recently, evidence for deficits in empathic responding

among youth with DBDs came primarily from studies of non-

verbal processing abilities and self-reported emotional empathy.

Nonverbal processing of affect, or the ability to read and decode

emotions in faces and vocal tones, is critical for social functioning

and is a principal component of empathy (Elfenbein, Marsh, &

Ambady, 2002). Children with DBDs are less accurate at de-

coding emotion in both faces and voices. For example, children

with psychopathic tendencies show selective impairments in the

recognition of both sad and fearful vocal tones and facial ex-

pressions (Stevens, Charman, & Blair, 2001). Furthermore, clin-

ically identified children diagnosed with CD do not decode

emotion in faces as well as age-matched controls (Strand & No-

wicki, 1999). Youth with DBDs also self-report lower emotional

arousal in response to affective pictures and describe fewer con-

cordant emotional responses to other’s expressions of affect,

particularly sadness and anger (de Wied et al. 2005; Douglas &

Strayer, 1996; Herpertz et al., 2005). These findings are not

surprising given the extent to which emotional sensitivity

conflicts with aggressive or otherwise delinquent acts that are

characteristic of these youth (Beauchaine, Gartner, & Hagen,

2000; Blair, 1995).

Among the various components of emotional responding,

facial expressions have emerged as a promising means of eval-

uating state reactivity to emotionally evocative stimuli and ap-

pear to be particularly relevant for studies of empathy (Ekman,

1992). Humans tend to unconsciously mimic facial expressions

that are congruent with the emotions they perceive, and this

mimicry appears to be important for efficiently and accurately

detecting emotional states in others (Niedenthal, Brauer,

Halberstadt, & Innes-Ker, 2001). Compared with simply

observing emotional subject matter, generating facial muscle

movements that imitate another’s emotional state evokes height-

ened activation in neural circuits that are implicated in the ex-

perience of emotion, such as the inferior frontal cortex, superior

temporal cortex, insula, and amygdala (Carr, Iacoboni, Dubeau,

Mazziotta, & Luigi Lenzi, 2003; Iacoboni, 2005). Thus, mimicry

may play an important role in the ability to empathize with the

emotions of others. Facial mimicry of sadness is of particular

interest, as it is important in emotional contagion, or vicariously

sharing the emotions of others, which is thought to precede

empathic responding (Hess & Blairy, 2001).

Although few studies have investigated facial expressions in

youth with DBDs, preliminary findings have begun to emerge.

While taking an IQ test, externalizing boys exaggerated facial

expressions of anger, but not of fear or sadness (Keltner,Moffitt,

& Stouthamer-Loeber, 1995). In contrast, facial mimicry of an-

gry facial expressions is limited among boys with DBDs, sug-

gesting that they may be deficient in their ability to identify with

angry emotional states in others (deWied, van Boxtel, Zaalberg,

Goudena, & Matthys, 2006). Thus, although preliminary

research suggests that facial expressions of sadness may not be

impaired in youth withDBDs, no research has investigated facial

sadness in these youth using tasks designed specifically to elicit

sad emotional states (Keltner et al., 1995). Thus, further research

is needed.

There is also evidence that viewing another person in dis-

tress elicits corresponding autonomic nervous system (ANS) re-

sponses that indicate emotional states (Eisenberg et al., 1988;

Levenson & Ruef, 1992; Tsai, Levenson, & Cartenson, 2000;

Walbott, 1991). These autonomic response patterns appear to be

consistent across cultures and serve to recruit the physiological

resources needed to regulate and respond to emotional cues

(Levenson, 1992; Levenson & Ruef, 1992). The ANS also

mediates expressive changes in the eyes and facial muscles that

are important for emotional communication (Levenson, 2003).

Thus, different patterns of ANS responding appear to be im-

portant for empathy reactions.

It is now well known that children and adolescents with

DBDs exhibit patterns of underresponsiveness in both the

sympathetic and parasympathetic branches of the ANS (e.g.,

Beauchaine, Gatzke-Kopp, &Mead, 2007; Beauchaine, Katkin,

Strassberg, & Snarr, 2001; Crowell et al., 2006; Ortiz & Raine,

2004). These findings extend to a number of stimulus conditions,

including (a) responding for monetary incentives, (b) viewing

escalating conflict scenes among child actors, and (c) viewing

both pleasant (pictures of pets or family scenes) and unpleasant

(pictures of wounded children and violent scenes) images (e.g.,

Beauchaine et al., 2001; Herpertz et al., 2005). In the only study

in which autonomic reactivity was assessed specifically during

distress cues in such a population, Blair (1999) reported lower

skin conductance responses to expressive emotional slides (e.g., a

person crying) among clinic-referred children with psychopathic

tendencies compared with controls. Although these same deficits

were not observed in boys with DBDs who did not exhibit

psychopathic traits, the sample size was limited, and only one

measure of autonomic activity (electrodermal responding) was

recorded. Thus, it remains unclear whether youth with DBDs

show broader patterns of deficient autonomic responding when

viewing others in distress. However, these findings suggest that

boys with DBDs may not show a more global pattern of abnor-

mal autonomic responding during sad emotional states.

In addition, research conducted with DBD samples to date

has focused almost exclusively on reactivity within single

Response dissociation and disruptive behavior disorders 101

emotional response systems. The few studies that have sampled

multiple domains of emotional responding among youth with

DBDs have indicated functional compromises across systems,

underscoring the importance of measuring multiple domains of

emotional reactivity. Children with CD, for example, self-report

low levels of arousal to unpleasant pictures and show autonomic

hyporesponsiveness to positive, negative, and neutral emotional

stimuli (Herpertz et al., 2005). Thus, although much progress

has been made in delineating the univariate emotional deficits

exhibited by youth with DBDs, it remains unclear how their

emotion response systems are coordinated. One possibility is

that certain deficits (such as responses to sadness) may not be

observable unless multiple response systems are considered.

In this study, we used multilevel modeling techniques to eval-

uate time-linked correspondence of facial expressions of sadness

and ANS reactivity in youth with DBDs and their typically

developing peers. We use the term correspondence somewhat

broadly to refer to time-linked correlations between any two

emotional response systems. This is the first study to apply a

multilevel modeling approach to questions of response coher-

ence. This procedure should bemore sensitive to detecting effects

than more traditional approaches given increased power associ-

ated with direct modeling of hierarchically structured data at all

levels of nesting (i.e., repeated measures nested within

individuals nested within groups).

In addition, although many theories of response coherence

are predicated on the fact that incoherent emotional responding

across systems marks ill health, to our knowledge this is the

first study to use such methodologically rigorous procedures to

test whether the level of coherence differs between individuals

with and without psychopathology. This study addresses a

critical hypothesisFthat boys with DBDs show less correspon-

dence across emotional response systems than control boysFre-

gardless of their overall levels of emotional responding. We

examined how emotional response systems are coordinated in

boys with DBDs and their age-matched peers during a sad emo-

tion induction. We hypothesized that boys with DBDs would

exhibit (a) fewer expressions of sadness, (b) less physiological

reactivity, and (c) less correspondence between facial expressions

of sadness and autonomic reactivity during an empathy-eliciting

film than controls.

Method

Participants

Data for this study were drawn from a larger investigation of the

autonomic substrates of childhood emotional and behavioral

problems. Parents of children were recruited through fliers,

newspaper ads, and community outpatient clinics serving sub-

urban and urban communities in and around Seattle, Washing-

ton. One version of these ads described the behavioral

characteristics of ODD and CD and informed parents that they

could earn $75 for participating with their child. A second ver-

sion recruited well-adjusted children. Parents of potential child

participants were interviewed by telephone using a computerized

diagnostic interview that included portions of the Child Symp-

tom Inventory (CSI; Gadow & Sprafkin, 1997). The parent ver-

sion of the CSI is a dimensionalized DSM-IV checklist with

established test–retest reliability and adequate predictive validity

compared with psychiatric diagnoses of ODD and CD (Gadow

& Sprafkin, 2002). Parent responses on the CSI also demonstrate

concurrent validity with the aggressive behavior and delinquency

subscales on the Child Behavior Checklist (CBCL; Achenbach,

1991). Ratings are rendered across four anchors (05 never,

15 sometimes, 25 often, 35 very often), with scores of 2 or

higher considered positive for each diagnostic criterion. Children

were considered positive for a given disorder if enough symptoms

were endorsed at 2 or higher to meet DSM-IV criteria.

Families were invited to participate if they met inclusion cri-

teria but failed to meet exclusion criteria for one of the study

groups. Boys were placed in the DBD group if they met diag-

nostic criteria for ODD and/or CD based on the CSI. Controls

were required to be diagnosis free on all CSI-assessed disorders.

Scores on all psychopathology scales are reported by group in

Table 1. Convergent evidence of psychopathology was obtained

from the CBCL, parent report (Achenbach, 1991). Scores ob-

tained on the CBCL aggression, attention, and anxious/de-

pressed scales are also reported by group in Table 1.

The sample included 31 boys with DBDs and 23 controls,

ranging in age from 9 to 13. The racial/ethnic composition in-

cluded 16.7% minority participants (7.4% African American,

3.7% American Indian, 1.9% Asian American, 3.8% other).

Parents reported a median family income of $50,000. Demo-

graphic information is reported in Table 1.

Procedure

Active informed consent was obtained from parents and youth

according to procedures approved by the University of Wash-

ington Human Subjects Review Committee. Participants were

instructed to avoid caffeine and over-the-counter medications

24 h prior to their visit. Participants were also asked to discon-

tinue stimulants (if applicable)Fmost of which have very short

half livesF36 h prior to the laboratory visit to minimize effects

on psychophysiological recordings. Use of other medications

was fairly low in this sample. Nine participants (16.7%) reported

stimulant use, 2 participants (3.7%) reported antidepressant use,

and 1 participant (1.9%) reported atomoxetine use. All analyses

were initially run with these boys dropped from the models and

then refit with them included. No significant differences were

observed between models, so only the models with all partic-

ipants included are presented. All information obtained from

participant families was protected by a Certificate of Confiden-

tiality from the National Institute of Mental Health.

During the visit, boyswere seated in a sound-attenuated room

and filmed by a concealed camera. Boys first participated in a

monetary incentive and extinction task that lasted approximately

30 min and has been described in detail elsewhere (e.g.,

Beauchaine et al., 2001). Then, following a 5-min baseline, par-

ticipants underwent the sad emotion induction procedure.1 This

involvedwatching a 3-min scene fromThe Champ, a film that has

been used extensively in prior research to elicit emotional sad-

ness, as indicated by subjective, behavioral, physiological, and

neural responses among both adolescents and adults (e.g.,

Crowell et al., 2005; Goldin et al., 2005; Gross & Levenson,

1995; Hewig et al., 2005; Hutcherson, Goldin, Ochsner, Gabrieli,

& Gross, 2005). The film shows a young boy responding to the

102 P. Marsh, T.P. Beauchaine, and B. Williams

1To determine whether there were carryover effects in the autonomicmeasures from the incentive task, we performed repeated measures an-alyses of variance in which (a) the last minute of responding during the5-min baseline before the incentive task and (b) the last minute of re-sponding during the 5-min baseline before the film were evaluated. Notime effects, group effects, or Group � Time interactions were found forPEP, SCL, or RSA.

death of his father. He reacts with disbelief and then becomes

increasingly inconsolable. For purposes of the present study, an

emotional film clip offered several advantages over other proce-

dures commonly used to elicit emotions, such as still picture

paradigms. Most importantly, we were interested in assessing

time-linked synchronization of emotional reactivity across au-

tonomic and facial channels, a goal that could not be accom-

plished efficiently using discrete stimulus presentations. Sadness

was targeted because the degree of sadness induced by viewing

another person in distress quantifies empathic responding, the

development of which is compromised among boys with behav-

ior problems (Duan, 2000; Eisenberg et al., 1988; Hess & Blairy,

2001). Boys’ psychophysiological responding across a number of

channels (see below)was continuously recorded during the video.

Families were recompensed $75 for participation.

Psychophysiological Measures

Skin conductance level (SCL). To assess electrodermal

responding during the task, SCL was acquired continuously us-

ing a Grass Model 15LT Physiodata Amplifier System with a

15A12 DC amplifier (West Warwick, RI). Two 0.8-cm2 Ag-AgCl

electrodes were applied to the thenar eminence of the partici-

pant’s nondominant hand using adhesive masking collars and

Parker Laboratories Signa Gel (Fairfield, NJ). The SCL signal

was recorded in microSiemens and digitized at 1 kHz using the

Grass PolyVIEW software system. Electrodermal responding

reflects cholinergically mediated influences of the sympathetic

nervous system (SNS). Increased SCL indicates SNS activation.

All SCL data were within-person centered for use in the

multilevel models, described below, to minimize hydration

artifacts (Ben-Shakhar, 1985).

Cardiac preejection period (PEP). Cardiac activity wasmon-

itored continuously during the task via electrocardiographic

(ECG) and impedance cardiographic (ICG) signals acquired by a

HIC 2000 Impedance Cardiograph (Chapel Hill, NC) using the

spot electrode configuration described by Qu, Zhang, Webster,

and Tompkins (1986). Both the ECG and ICG waveforms were

digitized at 1 kHz. Digitized ECG and ICG signals were ensem-

ble-averaged in 30-s epochs using COP-WIN 5.06. PEP was in-

dexed as the time between left-ventricular depolarization,

indicated by onset of the ECG Q-wave, and the initiation of

ejection of blood into the aorta, indicated by the ICG B-wave.

PEP is a validated measure of b-adrenergically mediated

SNS-linked cardiac activity (see Sherwood, Allen, Obrist, &

Langer, 1986; Sherwood et al., 1990). Shorter PEPs indicate

increased SNS activation.

Respiratory sinus arrhythmia (RSA). RSA was indexed by

extracting the high frequency component (40.15 Hz) of the

R-R time series using spectral analysis. High-frequency spectral

densities were calculated in 30-s epochs using the Medistar

Nevrokard software system and normalized through natural log

transformations, as is common practice. The ECG signal was

acquired through the ICG electrodes, which were arranged in a

Response dissociation and disruptive behavior disorders 103

Table 1. Descriptive Statistics for Boys in the Disruptive Behavior Disorder (DBD) and Control Groups

Variable DBD (n5 31) mean (SD) Control (n5 23) mean (SD) Effect size (d) F(1,52) p

Age 9.8 (1.4) 10.5 (1.5) 0.5 1.39 .24Family income (thousands) 52.3 (43.8) 66.4 (22.2) 0.4 2.77 .10Single parent homes 42% 19% 0.6 3.42 .07Minority status 23% 9% 0.4 1.83 .18CBCL aggression T score 79.2 (7.5) 50.8 (2.0) 5.2 310.00 o.01CBCL attention problems T score 74.2 (11.0) 52.9 (6.5) 2.4 68.46 o.01CBCL anxious/depressed T score 73.5 (10.6) 52.9 (3.8) 2.6 78.90 o.01CSI CD symptom count 2.3 (2.0) 0.0 (0.0) 1.6 28.71 o.01Diagnostic criteria met 51% 0%

CSI ODD symptom count 6.4 (1.6) 0.3 (0.7) 8.9 291.30 o.01Diagnostic criteria met 94% 0%

CSI ADHD symptom count 11.8 (4.4) 2.3 (3.4) 2.4 75.65 o.01Diagnostic criteria met 41% 0%

CSI MDD symptom count 1.3 (2.3) 0.0 (0.0) 0.8 8.23 o.01Diagnostic criteria met 10% 0%

CSI dysthymia symptom count 1.0 (1.8) 0.0 (0.0) 0.8 6.87 .01Diagnostic criteria met 23% 0%

Facial sadnessa

Baseline 0.4 (0.6) 0.2 (0.4) 0.4 2.23 .14Second-by-second scoring 0.3 (0.5) 0.4 (0.5) 0.2 1.20 .64Epoch scoring (30 s) 2.0 (1.4) 2.4 (1.8) 0.3 0.95 .34

Baseline physiological dataSkin conductance (mS) 0.03 (0.1) 0.05 (0.1) 0.2 1.21 .28Preejection period (ms) 102.3 (20.1) 99.3 (18.1) 0.2 0.32 .57Respiratory sinus arrhythmia (ms2) 9.1 (1.4) 9.1 (1.4) 0.0 0.00 .99

Task physiological datab

Skin conductance (mS) 0.3 (0.3) 0.6 (0.8) 0.3 F FPreejection period (ms) 105.5 (18.2) 100.1 (18.6) 0.3 F FRespiratory sinus arrhythmia (ms2) 9.1 (1.3) 9.3 (1.4) 0.2 F F

Notes. DBD: disruptive behavior disorder; CSI: Child Symptom Inventory; CD: conduct disorder; ODD: oppositional defiant disorder; ADHD:attention deficit hyperactive disorder; MDD: major depressive disorder.aFacial sadness values are not comparable across conditions given differences in scoring protocols.bGroup differences in physiological responding during the task are not presented here because they were evaluated in the multilevel models and arereported in text.

modified Lead II configuration. RSA is a well-validated measure

of parasympathetic nervous system (PNS) activity (see Berntson

et al., 1997). Increases in RSA reflect greater PNS activation.

Facial Sadness

Emotion elicitation condition. Videotapes of participants ob-

serving the film clip were coded by two trained research assistants

using the Emotional Behavior Coding System (EBCS; Gross,

1996). Coders were blind to participant diagnostic status and

were required to attend an 8-week training course prior to be-

ginning coding. During the training, coders were required to

learn the individual muscular actions and the prototype expres-

sion for sadness described by Ekman and Friesen (1975), which

serve as the basis for the EBCS codes. The sadness code of the

EBCS categorizes the degree of facial sadness expressed each

second based on the presence and valence (intensity) of emotion

expression. In accord with EBCS guidelines, coders first ob-

served the participant for 2 min at baseline to familiarize them-

selves with the participants’ natural resting facial expressions.

While coding, scores were assigned during the sad emotion in-

duction based upon movement away from this baseline. Sadness

was coded on a 4-point scale, including 0 (no sadness), 1 (slight

down turning of the mouth or a slight upturning of the inner eye-

brow), 2 (anymoderate sign of sadness, including clear upturning of

the inner eyebrow or mouth, slight quivering of the chin or mouth,

widening of the nostrils), and 3 (multiple moderate signs of sad-

ness). Scores were assigned each second to match the temporal

sequencing of the SCL data.

For PEP and RSA, which cannot be scored reliably on a

second-to-second basis, a single sadness value was assigned to

each 30-s epoch. This enabled us to match the timing of the

cardiac measures. To capture both the duration (number of sec-

onds spent appearing sad in the 30-s period) and the intensity of

sadness, codes were assigned on a scale of 0 (0 s spent showing any

signs of sadness) to 6 (at least 3 s showing multiple moderate signs

of sadness). For example, to obtain a 2 across the 30-s epoch,

participants needed to show at least 3 s of 1 level sadness within

that epoch. To obtain a 4 across the 30-s epoch, participants

needed to show at least 2 s of 2 level sadness within that epoch.

This coding scheme carries more information than a simple

average because it weights higher valenced (less subtle) facial

expressions of sadness more heavily.

Baseline condition. Because group differences in facial

sadness at baseline could affect outcomes observed during the

emotion elicitation, we also assessed facial expressions during the

5-min rest period preceding the task. This was accomplished

using amodified version of the ECBS procedure described above.

Global scores of facial sadness (rather than changes from base-

line) were assigned to each participant across the entire 5-min rest

period on a scale of 0 (no facial sadness) to 3 (multiple signs of

sadness).

To assess reliability, 15% of the data were assigned randomly

to both coders, who were unaware of which data were used for

assessing interrater agreement. The average between-observer

agreement, using a � 1-s window, was 89% for the second-by-

second data. The intraclass correlation coefficient was adequate

for both the second-by-second data (using a � 1-s window),

r5 .74, and for the 30-s windowed data, r5 .73. These reliabil-

ity statistics are consistent with prior research using the EBCS to

code facial displays of sadness (e.g., Rottenberg, Kasch, Gross,

& Gotlib, 2002).

Results

Preliminary Analyses

Descriptive statistics. Descriptive statistics for each measure

are reported by group in Table 1. Prior to analyses, distributions

of all variables were examined for adherence to distributional

assumptions of the inferential statistics used. Preliminary ana-

lyses evaluated the significance of group differences in each of the

psychopathology scales using analyses of variance (ANOVAs).

Effect sizes (Cohen’s d) are also reported. As expected, given our

recruitment strategy, group differences in CSI symptoms of

CD, ODD, hyperactivity, inattention, MDD, and dysthymia

were significant, all Fs46.87, ps � .01, with large effect sizes

(d5 0.8–8.9).

Baseline effects. During the 5-min baseline, there were no

significant differences in autonomic activity for any of the mea-

sures, all Fso3.03, all ps4.09 (see Table 1). In addition, few

expressions of facial sadness were observed at baseline for boys

withDBDs or for controls (see Table 1), with no group difference

found, F5 2.23, p5 .14.2

Multilevel Modeling Analyses

During the video clip, boys showed facial expressions of sadness

that were above baseline levels 22% of the time, which is con-

sistent with figures reported in prior research. This suggests that

the clip was effective in eliciting state sadness (see Rottenberg et

al., 2002). Next, analyses exploring group differences in levels of

each of the assessed measures were conducted using HLM 6.0

(Raudenbush, Bryk, Cheong, & Congdon, 2004). One of the

advantages of the multilevel modeling approach is that it pro-

vides simultaneous estimates of both within-participant effects

(e.g., the 180 repeated observations of SCL and facial sadness for

each person) and between-participants effects (e.g., individual

differences in the relationship between SCL and facial sadness

between people or between groups). Full maximum likelihood

models followed the general form presented below for facial

sadness:

Level 1: sadnessti ¼ p0i þ eti

Level 2: p0i ¼ b00 þ b01ðgroupiÞ þ uoi:

At Level 1 the repeated observations for each participant were

modeled. For example, in the equation above, sadnessti repre-

sents the 180 repeated observations of sadness (one observation

per second for 3 min) for each person. At Level 2, individual

variation among participants was assessed, and group compar-

isons were conducted using a dummy coded time invariant vari-

able (15DBD, 05 control). Thus, in the Level 2 equation

above, the b01 term captures whether there are differences be-

tween groups in average levels of sadness. This set of analyses

tested the hypotheses that boys with DBDs would exhibit (a)

fewer expressions of sadness and (b) less physiological reactivity

than controls. No significant group differences were found on

104 P. Marsh, T.P. Beauchaine, and B. Williams

2For investigative purposes, we also explored whether other forms ofemotion (e.g., contemptuous affect) differed between groups. Fifteenpercent of the boys showed transient expressions ofmild contempt duringthe video (unilateral lip raise, eye roll), which typically lasted less than 5 s.However, there were no significant differences in contempt displayedbetween groups. Furthermore, we considered whether contemptuousaffect interacted with diagnostic group status to predict patterns of au-tonomic responding in models paralleling those described for sadnessabove. No such effects were found.

any of the assessedmeasures: sadness, b01 5 � .34, p5 .34; SCL,

b01 5 .07, p5 .54; PEP, b01 5 � 5.37, p5 .30; RSA, b01 5

� .12, p5 .75. Thus, contrary to the first two study hypotheses,

boys with DBDs and controls showed similar levels of facial

sadness, SCL, PEP, and RSA during the emotion induction.

Demographic effects. Correlational analyses were used to

examine the relations among (a) mean levels of facial sadness,

(b) mean levels of each of the psychophysiological measures

during the emotion induction, (c) adolescents’ racial/ethnic

groupmembership, and (d) family income. This ensured that any

observed effects were not artifacts of demographic differences

within the sample. Results indicated no significant effects for

race/ethnicity or parental income on the assessed variables (all

rso.20, all ps4.14). Demographic variables were therefore

omitted from further analyses in order to maximize power.

Response coherence analyses. HLM with full maximum like-

lihood estimation was used to compare the response coherence of

groups.3 For each psychophysiological measure, a two-level

model was constructed (Bryk & Raudenbush, 1992). The SCL

model was as follows:

Level 1: SCLti ¼ p0i þ p1iðtimetiÞ þ p2iðsadnesstiÞ þ eti

Level 2:p0i ¼ b00 þ b01ðgroupiÞ þ uoi

p1i ¼ b10 þ b11ðgroupiÞ þ u1i

p2i ¼ b20 þ b21ðgroupiÞ þ u2i:

At Level 1 the relationship between facial sadness and SCL

was assessed by modeling the 180 second-by-second repeated

observations of SCL and facial expression data for each partic-

ipant, with facial sadness included as a time-varying covariate.

At Level 2, variation in coherence among individuals was as-

sessed, and group comparisons were conducted using a dummy

coded time invariant variable (15DBD, 05 control).

Identical procedures were followed for PEP and RSA, with

two exceptions. First, because PEP and RSA were scored in 30-s

epochs, data were modeled across the six 30-s epochs rather than

across seconds. Second, because the time effect was not signifi-

cant when added to the Level 1 equation in either model (PEP:

b10 5 .22, p5 .23; RSA: b10 5 .00, p5 .76), the term was

dropped in order to correctly identify the Level 1 model while

maximizing degrees of freedom (Bryk & Raudenbush, 1992).

The final RSA model is shown below:

Level 1: RSAti ¼ p0i þ p1iðsadnesstiÞ þ eti

Level 2:p0i ¼ b00 þ b01ðgroupiÞ þ uoi

pli ¼ b10 þ b11ðgroupiÞ þ uli:

Analyses revealed significant associations between facial sad-

ness and (a) decreased SCL, b20 5 � .09, p5 .03; (b) lengthened

PEP, b10 5 1.19, po.001; and (c) increased RSA, b10 5 .09,

p5 .02. Thus, expressions of sadness were associated with re-

duced SNS and increased PNS activity. However, each of these

findings was moderated by a significant group effect: SCL,

b21 5 .15, p5 .01; PEP, b11 5 � 1.04, po.01; RSA, b11 5 � .13,

p5 .03. Associations between facial sadness and autonomic re-

sponding are depicted by group in Figure 1. These findings are

consistent with our third hypothesis, that boys withDBDswould

exhibit less correspondence between facial expressions of sadness

and autonomic reactivity to the emotion induction.

Follow-up group contrasts indicated that for each variable,

significant associations between facial expression and autonomic

responding were observed among controls, all pso.05, but not

among boys with DBDs, all ps � .49. Without these contrasts,

we could not rule out the possibility that boys with DBDs ex-

hibited significant, albeit diminished, coherence relative to con-

trols. Thus, controls evidenced a pattern of response coherence

in which the PNS was activated and the SNS was deactivated

during expressions of sadness. In contrast, facial expressions and

autonomic responses were not significantly related for boys with

DBDs. Effect sizes (Cohen’s d) separating boys with DBDs from

controls on HLM slopes, which represent the correspondence

between facial expressions and autonomic responding, were .70

for SCL, .87 for PEP, and .40 for RSA.

As is often the case, a greater number of boys withDBDswere

symptomatic for ADHD (42%) and depression (7%) than con-

trols (0% and 0%, respectively). Given this, we also explored

whether the effects reported above were independently attribut-

able to DBDs, above any effects of MDD, dysthymia, and

ADHD. To accomplish this, allmodels were rerunwith scores for

(1) MDD, then (2) dysthymia, and finally (3) hyperactivity add-

ed as Level 2 time-invariant covariates for each of the psycho-

physiological measures.MDD, dysthymia, and hyperactivity did

not moderate the relationships between facial sadness and any of

the assessed autonomic indices. Moreover, all but one group

difference in the relationship between facial sadness and the

physiological measures remained significant after controlling for

MDD (SCL, b21 5 .14, p5 .03; PEP, b11 5 � 1.09, po.01;

RSA, b11 5 .14, p5 .03), dysthymia (SCL, b21 5 .14, p5 .03;

PEP, b11 5 � 1.06, po.01; RSA, b11 5 � .13, p5 .04), and

ADHD (SCL, b21 5 .15, p5 .03; PEP, b11 5 � 1.04, po.01;

RSA, b11 5 � .10, p5 .12).4

Relation between Response Coherence and Problem Behaviors

In our final set of analyses, we evaluated associations between

response coherence and measures of both internalizing and ex-

ternalizing psychopathology. These analyses are summarized in

Table 2, where we present correlations between individual slopes

obtained from the HLM analyses, which represent response co-

herence, and each of the problem behavior scales from the CSI.

These analyses yielded an interesting pattern of results. First,

PEP slopes were negatively correlated with all externalizing be-

havior scores, including CD, ODD, hyperactivity, and inatten-

tion. Because response coherence for PEP was signified by

positive slopes (see Figure 1), this indicates that low correspon-

dence between PEP reactivity and facial expressions of sadness

were associated with externalizing behaviors. No such pattern

was observed linking PEP to internalizing behaviors.

Second, in direct contrast with the findings for PEP, RSA

slopes were negatively correlated with all internalizing behavior

Response dissociation and disruptive behavior disorders 105

3For the HLM analyses, exact p values are reported for all proba-bilities at or above .001. Because HLM does not provide exact p valuesbelow this level, these effects are indicated by the inequality po.001.

4In a separate series of analyses, minority status and single parentstatuswere entered as Level 2 time invariant covariates into all analyses toexamine whether the reported effects were moderated by demographicfactors. Neither demographic variable altered the relationships betweenfacial sadness and any of the assessed autonomic indices. Moreover,group differences in the relationship between facial sadness and each ofthe physiological indicators remained after controlling forminority status(SCL, b21 5 .14, p5 .03; PEP, b11 5 � 1.02, p5 .00; RSA, b11 5 � .14,p5 .03), and single parent status (SCL, b21 5 .14, p5 .03; PEP,b11 5 � .99, p5 .01; RSA, b11 5 � .13, p5 .06).

scores, including major depression and dysthymia. Because re-

sponse coherence for RSA was also signified by positive slopes

(see Figure 1), this indicates that low correspondence between

RSA reactivity and facial expressions of sadness were associated

with internalizing behaviors. No such pattern was observed link-

ing RSA reactivity to externalizing behaviors. Thus, response

dissociation between PEP reactivity and facial expressions was

specific to externalizing behaviors, whereas response dissociation

between RSA reactivity and facial expressions was specific to

internalizing behaviors.

Third, SCL slopes were positively correlated with all inter-

nalizing and externalizing behavior scores. Because response

coherence for SCL was indexed by negative slopes (see Figure 1),

this indicates that low correspondence between SCL reactivity

and facial expressions of sadness were associated with both

internalizing and externalizing outcomes.

Finally, we computed partial correlations between response

coherence slopes and each externalizing measure (e.g., CD),

controlling for all others (e.g., ODD, hyperactivity, inattention),

and between response coherence slopes and each internalizing

measure (e.g., MDD), controlling for the other (e.g., dysthymia).

None of these partial correlations, which represent the indepen-

dent effects of each psychopathology scale in predicting response

coherence, were significant. Thus, the pattern of results summa-

rized above applies broadly to externalizing and internalizing

symptoms and not to any specific diagnostic class.

Discussion

In this study, we evaluated three hypotheses regarding facial ex-

pressions and autonomic responses of boyswithDBDs during an

empathy-eliciting film. First, we predicted fewer expressions of

sadness to the scene of a boy with his dying father among boys

with DBDs than among controls. This hypothesis was not sup-

ported. Boys with DBDs and controls demonstrated equivalent

levels of facial sadness, both at baseline and during the film.

Although the null finding at baseline is not surprising given the

absence of eliciting stimuli, we expected a group difference during

emotion induction, following from previous research demon-

strating empathy deficits in boys with DBDs. Second, we pre-

dicted less physiological reactivity to the film among boys with

DBDs than among controls, also marking expected deficits in

empathy. This hypothesis was also unsupported.

106 P. Marsh, T.P. Beauchaine, and B. Williams

Table 2. Bivariate (and Partial) Correlations between Response

Coherence Slopes and Problem Behavior Scores

Variable PEP slope SCL slope RSA slope

Physiological measuresPEP slope FSCL slope � .23 FRSA slope � .25 � .15 F

Externalizing scalesASI conduct

disorder� .31n (� .09) .32n (� .02) � .21 (� .03)

ASI oppositionaldefiant disorder

� .33n (� .02) .34n (� .12) � .17 (.20)

ASI hyperactivity � .35n (� .09) .32n (� .19) � .06 (� .06)ASI inattention � .37n (.21) .31n (.10) � .11 (� .12)

Internalizing measuresASI major

depressive disorder� .16 (.04) .31n (.01) � .32n (� .20)

ASI dysthymia � .13 (� .11) .35n (� .05) � .37n (.25)

Notes. PEP: preejection period; SCL: skin conductance level; RSA: re-spiratory sinus arrhythmia; ASI: Adolescent Symptom Inventory (scalescores). Slopes represent the correspondence between each autonomicmeasure (PEP, SCL, RSA) and facial expressions of sadness during thefilm. These slopes were extracted from the HLM analyses for each par-ticipant. Partial correlations reflect the correspondence between responsecoherence slopes and each externalizing measure, controlling for all oth-ers, and each internalizing measure, controlling for the other.np � .05, two-tailed.

96

98

100

102

104

106

108

110

0 1 2 3 4 5 6

00 1 2 3

8.8

9.0

9.2

9.4

9.6

9.8

0.8

0.6

0.4

0.2

SC

L (m

icro

sie

men

s)

Facial Sadness

Control

DBD

Control

DBD

PE

P (

ms)

Control

DBD

RS

A (

In(m

s2))

Facial Sadness

0 1 2 3 4 5 6Facial Sadness

Figure 1. Associations between facial expressions of sadness and skin

conductance level (SCL; top panel), preejection period (PEP; middle

panel), and respiratory sinus arrhythmia (RSA; bottom panel) for boys

with DBDs (dashed lines) and controls (solid lines). Note that facial

sadness ranged from 0 (no sadness) to 3 (highest level of sadness) for SCL,

and from 0 (no sadness) to 6 (highest level of sadness) for PEP and RSA

because of the different temporal resolutions of measures.

One possible interpretation of these findings is that the film

clip was ineffective in eliciting empathy among participants, re-

gardless of their group status. However, several previous studies

have demonstrated the effectiveness of theThe Champ in evoking

state sadness (Crowell et al., 2005; Goldin et al., 2005; Gross &

Levenson, 1995; Hewig et al., 2005; Hutcherson et al., 2005).

Furthermore, even though group differences in facial expressions

and autonomic reactivity were not observed during the film, both

groups demonstrated increased facial sadness and altered auto-

nomic functioning compared with baseline. Thus, more likely

explanations for the failure to find group effects are (a) differ-

ences in the sample recruited for this study compared with pre-

vious studies and (b) divergent methods used in this study

compared with previous work.

Most data demonstrating empathy deficits in boys with

DBDs have been either behavioral or self-report. In one of the

few studies in which autonomic reactivity during a sad emotion

induction was measured, no group differences between children

with DBDs and controls in either RSA or heart rate emerged

(Zahn-Waxler, Cole, Welsh, & Fox, 1995). In fact, we are aware

of no findings linking deficient autonomic responding to deficits

in empathy observed during emotion induction using films. In

studies where empathy has been linked with autonomic respond-

ing among children, the relation has usually been correlational

and indirect (e.g., boys with DBDs have generalized low auto-

nomic arousal and exhibit limited empathy; Eisenberg et al.,

1996). Moreover, although Liew et al. (2003) did measure skin

conductance and heart rate, linking lower reactivity in each to

less empathy, this study (a) was conducted with a normative

sample and (b) linked ratings of empathy to autonomic reactivity

to static facial expressions of emotion (slides). Finally, although

Blair (1999) described a similar finding with skin conductance in

youth scoring high on psychopathy, such individuals comprise a

small subset of youth with DBDs who are especially recalcitrant

(see, e.g., Fowles & Dindo, 2006). In fact, Blair found no sig-

nificant differences in electrodermal responses to sad facial cues

between controls and boys withDBDs who did not score high on

psychopathy. Taken together, these findings suggest that boys

with DBDs may not differ from controls in overall patterns of

sympathetic or parasympathetic activity during the experience of

sadness.

The finding of similar levels of facial sadness in boys with

DBDs and controls during the emotion induction is also consis-

tent with research showing comparable levels of facial sadness in

externalizing and control boys during structured social interac-

tions (Keltner et al., 1995). Although previous research has re-

ported deficient facial reactivity to angry faces in youth with

DBDs, this study is the first to explore facial reactions to a sad

emotion induction, which may be more relevant to empathic

responding (de Wied et al., 2006). There is now reasonable

agreement that the vicarious experience of anger verses sadness

evokes different physiological and neurological responses. For

example, observing angry facial expressions is associated with

activity in the right orbitofrontal and cortex, whereas viewing sad

faces is associated with enhanced activity in the left amygdala

(Blair, Morris, Frith, Perrett, & Dolan, 1999). Anger and sad-

ness also evoke distinct autonomic reactions (Levenson, 1992)

and have distinct social communicative functions. Anger conveys

disapproval and signals others to withdraw, whereas sadness

elicits comfort and support from others (Izard, 1991). Thus, the

possibility that boys with DBDs are impaired in their facial re-

actions to angry but not sad emotional cues suggests that differ-

ent biological and communicative mechanisms may be involved.

Further research is needed to understand the mechanistic pro-

cesses involved in these deficiencies.

Our third and final hypothesis was that boys with DBDs

would exhibit less correspondence between facial expressions of

sadness and autonomic reactivity during an empathy-eliciting

film than controls. For all three autonomic measures, this hy-

pothesis was supported. During the emotion induction, facial

expressions of sadness were associated with reduced SNS activity

(lower SCLs, lengthened PEPs) and increased PNS activity

(higher RSA) among controls. In contrast, time-linked corre-

spondence between facial expressions of sadness and autonomic

reactivity was not observed among boys with DBDs. These

findings cannot be attributed to a lack of emotional responding

among boys with DBDs given that both groups exhibited similar

levels of sad facial expressions and autonomic reactivity during

the emotion induction. One way to interpret these findings is that

when boys with DBDs communicate sadness facially, the auto-

nomic nervous system is not responding adaptively to promote

physiological homeostasis and facilitate social engagement be-

haviors (cf. Porges, 1995, 1997, 2001).

Taken together, these results replicate those observed among

adults, suggesting that correspondence among emotional re-

sponse systems reflects adaptive emotional processing, perhaps in

part because emotional reactions are most efficient when discrete

systems work collectively (Mauss et al., 2005). These findings

provide some of the first empirical evidence that boys withDBDs

exhibit deficiencies in the correspondence of affect-modulating

systems that are necessary for effective emotion regulation. Had

we examined only one system (e.g., facial sadness or the auto-

nomic measures alone) these findings would not have been ev-

ident. This illustrates the importance of exploring multiple

measures of emotional responding concurrently and demon-

strates a potential role for emotional response coherence in elu-

cidating emotional deficits among boys with DBDs.

Significant links between facial expressions of sadness and

PNS-linked cardiac reactivity were not observed among boys

with DBDs. Given evidence for RSA as a peripheral index of

emotion regulation capabilities (e.g., Beauchaine, 2001; Beau-

chaine et al., 2007; Porges, 1995, 1997, 2001, 2007), this discor-

dance may indicate that physiological dysregulation plays a

central role in the inappropriate affect often displayed by youth

with DBDs. In normal samples, expressions of emotion are ac-

companied by changes in RSA, with aberrant patterns of RSA

and RSA reactivity observed among antisocial youth at baseline

and during negative emotion induction (e.g., Beauchaine et al.,

2001, 2007). The present study extends these findings and dem-

onstrates that boys with DBDs fail to exhibit changes in RSA

that are coordinated with their facial reactions to sad emotional

stimuli. Vagal influences, as indexed by RSA, typically modulate

sympathetic activity under conditions of emotional challenge

(Porges, 1995, 1997, 2001, 2007). With neurobiological and

facial reactions that are decoupled, boyswithDBDsmay lack the

resources to effectively modulate their physiological arousal,

rendering them less capable of responding appropriately to

others’ distress (Fabes, Eisenberg, & Eisenbud, 1993).

Phylogenetic accounts of emotion regulation suggest that

PNS-mediated strategies for modulating affect are preferred

among mammals. When unsuccessful, emotional lability pre-

vails, with the SNS driving behavior toward either fight or flight

responding, an evolutionarily older strategy (see Beauchaine

et al., 2007; Porges, 1995, 2007). In the present study, boys with

Response dissociation and disruptive behavior disorders 107

DBDs exhibited deficits in the coordination of facial expressions of

sadness and both PNS and SNS activity, which may mark ab-

normalities in emotion regulation capacities. Thus, combined PNS

and SNS deficiencies during moments of emotional expression

may have significant ramifications for emotional functioning.

Analyses evaluating the strength of correspondence between

emotional response coherence and individual psychopathology

scales yielded an interesting pattern of results, which can be

summarized as follows: (1) Deficits in response coherence be-

tween facial sadness and PEP were correlated exclusively with

externalizing symptoms, including CD, ADHD, and ODD; (2)

deficits in response coherence between facial sadness and RSA

were correlated exclusively with internalizing symptoms, includ-

ing major depression and dysthymia; and (3) deficits in response

coherence between facial sadness and SCL were correlated with

both externalizing and internalizing symptoms.

Because this pattern of results was not predicted and should

therefore be replicated before being considered robust, we are

reluctant to offer strong interpretations. Nevertheless, limited

speculation is warranted. Prediction of externalizing symptoms

by deficits in response coherence between facial sadness and PEP

adds to a growing body of literature linking SNS deficiencies

specifically to DBDs (e.g., Beauchaine et al., 2001, 2007). One

possible yet tentative interpretation is that functional deficiencies

within the dopaminergically mediated approach motivational

systemFwhich may be indicated by PEP changes to specific

stimuli (Beauchaine et al., 2007; Brenner, Beauchaine, & Sylvers,

2005)Fare reflected in response desynchrony. The approach

motivational system mediates both appetitive and active avoid-

ance behaviors, the latter of which facilitate escape from danger

and threat (see Beauchaine, 2001; Beauchaine et al., 2001). In the

present context, it is possible that sadness cues are not eliciting

active avoidance motivations among children with DBDs.

Again, this conjecture is speculative and requires further study.

Prediction of internalizing symptoms by deficits in response

coherence between facial sadness and RSA is consistent with a

growing literature linking vagal deficiencies to depressive, anx-

ious, and self-injurious behaviors (e.g., Crowell et al. 2005; Rot-

tenberg, Salomon, Gross, & Gotlib, 2005; Thayer, Friedman, &

Borkovec, 1996). Yet reduced RSA is also observed consistently

among externalizing children and adolescents (Beauchaine et al.,

2001, 2007; Mezzacappa et al., 1997). Thus, replication of this

finding is especially important before any claims of specificity to

depressive symptoms are offered.

Finally, prediction of both externalizing and internalizing

symptoms by deficits in response coherence between facial sad-

ness and SCL is consistent with findings linking deficient elec-

trodermal responding to both antisocial behavior and depression

(e.g., Lorber, 2004; Sponheim, Allen, & Iacono, 1995). It is also

well known that EDR is exquisitely sensitive to many types of

stimuli, regardless of positive or negative valence (Dawson,

Schell, & Filion, 2000). Again, we await future replications

before offering a stronger interpretation.

Taken together, findings linking response dysynchrony to

psychopathology must be juxtaposed with findings of no group

differences in physiological reactivity to the emotion induction.

Examination of descriptive statistics indicates the nonsignificant

group differences in physiological measures were all in the

expected directionFboth at baseline and during the emotion

inductionFwith the DBD group exhibiting lower skin conduc-

tance, longer preejection periods, and lower RSA than controls.

However, effect sizes were too small to reach statistical signifi-

cance. In contrast, effect sizes for differences in response coher-

ence were all large. This discrepancy in effect sizes may reflect

well-documented advantages of growth curve modeling, which

HLM uses in the Level 1 models, over more traditional ap-

proaches to evaluating group differences in repeated measures

over time (e.g., Rogosa, Brandt, & Zimowski, 1982; Speer &

Greenbaum, 1995). If this is the case, evaluations of response

coherence usingmultilevelmodelingmay offer an advantage over

traditional methods in differentiating among clinical groups

using physiological markers.

Limitations

Although this study advances our understanding of the relation

between facial expressions of sadness and autonomic reactivity

by assessing multiple response systems, there are nonetheless a

number of limitations to consider. First, the sample size was

relatively small, and the data were cross sectional. Consequently,

wewere unable to determine whether the pattern of results would

have been different had we recruited boys with only ODD versus

those with CD, the latter of whom tend to be older. Future

longitudinal studies are needed to assess howpatterns of response

coherence change throughout childhood and adolescence for

boys with DBDs. Second, the stimulus used elicited a particular

type of emotionFsadness/empathy. Research suggests that

different emotions generate specific ANS reactions (see Leven-

son, 1992). Using tasks designed specifically to elicit other emo-

tions such as anger may elaborate patterns of response coherence

and dysynchrony found in this study. Third, we focused on a

particular form of psychopathologyFDBDs. Future research

exploring multiple and distinct psychopathological conditions

(e.g., depression, anxiety, bipolar disorder) will help to uncover

whether a lack of correspondence is a general marker of psy-

chopathology or, alternatively, whether different patterns of in-

coherence are specific to different psychopathological conditions.

In addition, the lack of data from girls precluded exploration

of potentially important sex differences in emotional response

coherence. Moreover, although there is ample evidence for the

reliability and validity of parental reports of behavior problems

on the CSI, these data are were nonetheless limited by reliance on

a single informant. Furthermore, we examined correspondence

between two specific dimensions of emotional respond-

ingFANS patterns and facial reactivity. Future research might

address whether the patterns observed in this study are also

found when other emotional response domains (e.g., self-report

measures, EEG) are considered. Finally, we did not perform

time-lagged analyses, which could uncover alternative patterns

of response coherence across groups. For example, it is possible

that boys with DBDs exhibit slower autonomic reactions to the

experience of sadness, which might be detected by adding a

time-lagged component to the HLM analyses. Although such a

finding would be informative, it would not diminish findings

presented here demonstrating clear differences in immediate

response coherence among groups.

Conclusions

The results of this study indicate that although boys with DBDs

show appropriate levels of facial and autonomic responding to

elicitors of sadness, these systems are not as efficiently coupled as

they are among controls. Such findings are consistent with func-

tionalist theories of emotion, which argue that coordination

across response systems should be associated with positive

psychological adjustment and adaptive responding to social and

108 P. Marsh, T.P. Beauchaine, and B. Williams

environmental challenges. Although it has often been asserted

that emotion response systems subserve adaptation, there has

been little data on this question to date. In fact, our study may be

the first to conduct this type of analysis using sophisticated mul-

tilevel modeling procedures to assess response coherence. Con-

sidered collectively, our results highlight the value of evaluating a

broader array of emotional response systems than is typically

examined in studies that focus on either biological or expressive

components of emotional responding. Indeed, when multiple

response systems are considered, it is possible to discriminate

between boys with behavior problems and their age-matched,

typically developing peers. Had we examined any particular

emotional response system in isolation, these patterns would not

have been evident.

REFERENCES

Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18and 1991 Profile. Burlington, VT: University of Vermont Departmentof Psychiatry.

Achenbach, T. M., & Howell, C. T. (1993). Are American children’sproblems getting worse? A 13-year comparison. Journal of the Amer-ican Academy of Child & Adolescent Psychiatry, 32, 1145–1154.

American Psychiatric Association. (2000). Diagnostic and statisticalmanual of mental disorders (4th ed., text revision). Washington, DC:Author.

Beauchaine, T. P. (2001). Vagal tone, development, and Gray’s motiva-tional theory: Toward an integrated model of autonomic nervoussystem functioning in psychopathology. Development and Psychopa-thology, 13, 183–214.

Beauchaine, T. P., Gartner, J. G., & Hagen, B. (2000). Comorbid de-pression and heart rate variability as predictors of aggressive andhyperactive symptom responsiveness during inpatient treatment ofconduct-disordered, ADHD boys. Aggressive Behavior, 26, 425–441.

Beauchaine, T. P., Gatzke-Kopp, L., & Mead, H. K. (2007). Polyvagaltheory and developmental psychopathology: Emotion dysregulationand conduct problems from preschool to adolescence. BiologicalPsychology, 74, 174–184.

Beauchaine, T. P., Katkin, E. S., Strassberg, Z., & Snarr, J. (2001).Disinhibitory psychopathology in male adolescents: Discriminatingconduct disorder from attention-deficit/hyperactivity disorderthrough concurrent assessment of multiple autonomic states. Journalof Abnormal Psychology, 110, 610–624.

Ben-Shakhar, G. (1985). Standardization within individuals: A simplemethod to neutralize individual differences in psychophysiologicalresponsivity. Psychophysiology, 22, 292–299.

Berntson, G. G., Bigger, J. T., Eckberg, D. L., Grossmann, P., Kaufm-ann, P. G., & Malik, M., et al. (1997). Heart rate variability: Origins,methods, and interpretive caveats. Psychophysiology, 34, 623–648.

Berntson, G. G., Cacioppo, J. T., Quigley, K. S., & Fabro, V. T. (1994).Autonomic space and psychophysiological response. Psychophysiol-ogy, 31, 44–61.

Blair, R. J. R. (1995). A cognitive developmental approach to morality:Investigating the psychopath. Cognition, 57, 1–29.

Blair, R. J. R. (1999). Responsiveness to distress cues in the child withpsychopathic tendencies. Personality and Individual Differences, 27,135–145.

Blair, R. J. R., Morris, J. S., Frith, C. D., Perrett, D. I., & Dolan, R. J.(1999). Dissociable neural responses to facial expressions of sadnessand anger. Brain, 122, 883–893.

Brenner, S. L., Beauchaine, T. P., & Sylvers, P. D. (2005). A comparisonof psychophysiological and self-report measures of BAS and BIS ac-tivation. Psychophysiology, 42, 108–115.

Bryk, A. S., & Raudenbush, S. W. (1992).Hierarchical linear models forsocial and behavioral research: Applications and data analysis methods.Newbury Park, CA: Sage.

Buck, R. (1977). Nonverbal communication of affect in preschool chil-dren: Relationships with personality and skin conductance. Journal ofPersonality and Social Psychology, 35, 225–236.

Cacioppo, J. T., Uchino, B. N., & Berntson, G. G. (1994). Individualdifferences in the autonomic origins of heart rate reactivity: Thepsychometrics of respiratory sinus arrhythmia and pre-ejection peri-od. Psychophysiology, 31, 412–419.

Carr, L., Iacoboni, M., Dubeau, M., Mazziotta, J. C., & Luigi Lenzi, G.(2003). Neural mechanisms of empathy in humans: A relayfrom neural systems for imitation to limbic areas. Proceedings of theNational Academy of Sciences, USA, 100, 5497–5502.

Crowell, S., Beauchaine, T. P., Gatzke-Kopp, L., Sylvers, P., Mead, H.,& Chipman-Chacon, J. (2006). Autonomic correlates of attention-

deficit/hyperactivity disorder and oppositional defiant disorder inpreschool children. Journal of Abnormal Psychology, 115, 174–178.

Crowell, S., Beauchaine, T. P., McCauley, E., Smith, C., Stevens, A. L.,& Sylvers, P. (2005). Psychological, autonomic, and serotonergiccorrelates of parasuicidal behavior in adolescent girls. Developmentand Psychopathology, 17, 1105–1127.

Dawson, M. E., Schell, A. M., & Filion, D. L. (2000). The electrodermalsystem. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.),Handbook of psychophysiology (pp. 200–222). New York: CambridgeUniversity Press.

de Wied, M., Goudena, P. P., & Matthys, W. (2005). Empathy in boyswith disruptive behavior disorders. Journal of Child Psychology andPsychiatry, 46, 867–880.

de Wied, M., van Boxtel, A., Zaalberg, R., Goudena, P. P., & Matthys,W. (2006). Facial EMG responses to dynamic emotional facialexpressions in boys with disruptive behavior disorders. Journal ofPsychiatric Research, 40, 112–121.

Douglas, C., & Strayer, J. (1996). Empathy in conduct-disordered andcomparison youth. Developmental Psychology, 32, 988–998.

Duan, C. (2000). Being empathic: The role of motivation to empathizeand the nature of target emotions.Motivation andEmotion, 24, 29–50.

Eisenberg, N., Fabes, R. A., Murphy, B., Karbon, M., Smith, M., &Maszk, P. (1996). The relations of children’s dispositional empathy-related responding to their emotionality, regulation, and social func-tioning. Developmental Psychology, 32, 195–209.

Eisenberg, N., Schaller, M., Fabes, R., Bustamante, D., Mathy, R., &Shell, R., et al. (1988). Differentiation of personal distress and sym-pathy in children and adults.Developmental Psychology, 24, 766–775.

Ekman, P. (1992). An argument for basic emotions. Cognition and Emo-tion, 6, 169–200.

Ekman, P., & Friesen, W. V. (1975). Unmasking the face. EngelwoodCliffs, NJ: Prentice-Hall.

Elfenbein, H. A., Marsh, A., & Ambady, N. (2002). Emotional intel-ligence and the recognition of emotion from the face. In L. F. Barrett,& P. Salovey (Eds.), The wisdom of feelings: Processes underlyingemotional intelligence (pp. 37–59). New York: Guilford Press.

Fabes, R. A., Eisenberg, N., & Eisenbud, L. (1993). Behavioral andphysiological correlates of children’s reactions to others in distress.Developmental Psychology, 29, 655–663.

Feldman-Barrett, L. (2006). Are emotions natural kinds? Perspectives onPsychological Science, 1, 28–58.

Fowles, D. C., & Dindo, L. (2006). A dual-deficit model of psychopathy.In C. J. Patrick (Ed.), Handbook of psychopathy (pp. 14–34). NewYork: Guilford Press.

Gadow, K. D., & Sprafkin, J. (1997). Child Symptom Inventory 4 normsmanual. Stony Brook, New York: Checkmate Plus.

Gadow, K. D., & Sprafkin, J. (2002). Child Symptom Inventory 4:Screening and norms manual. Stony Brook, NY: Checkmate Plus.

Goldin, P. R., Cendri, A. C., Hutcherson, C. A., Ochsner, K. N., Glover,G.H., &Gabrieli, J. D. E., et al. (2005). The neural bases of amusementand sadness: A comparison of block contrast and subject-specificemotion intensity regression approaches. NeuroImage, 27, 26–36.

Gross, J. J. (1996). Emotion Expressive Behavior Coding System. Stan-ford, CA: Stanford University.

Gross, J. J., John, O., & Richards, J. (2000). The dissociation of emotionexpression from emotion experience: A personality perspective. Per-sonality and Social Psychology Bulletin, 26, 712–726.

Gross, J. J., & Levenson, R. W. (1993). Emotional suppression: Phys-iology, self-report, and expressive behavior. Journal of Personalityand Social Psychology, 64, 970–986.

Gross, J. J., & Levenson, R. W. (1995). Emotion elicitation using films.Cognition and Emotion, 9, 87–108.

Response dissociation and disruptive behavior disorders 109

Gross, J. J., & Levenson, R.W. (1997). Hiding feelings: The acute effectsof inhibiting negative and positive emotion. Journal of AbnormalPsychology, 106, 95–103.

Herpertz, S. C.,Mueller, B., Qunaibi,M., Lichterfeld, C., Konrad, K., &Herpertz-Dahlmann, B. (2005). Response to emotional stimuli inboys with conduct disorder. American Journal of Psychiatry, 162,1100–1107.

Hess, U., & Blairy, S. (2001). Facial mimicry and emotional contagion todynamic emotional facial expressions and their influence on decodingaccuracy. International Journal of Psychophysiology, 40, 129–141.

Hewig, J., Hagemann, D., Seifert, J., Gollwitzer, M., Naumann, E., &Bartussek, D. (2005). A revised film set for the induction of basicemotions. Cognition and Emotion, 19, 1095–1109.

Hutcherson, C. A. C., Goldin, P. R., Ochsner, K. N., Gabrieli, J. D. E.,& Gross, J. J. (2005). Attention and emotion: Does rating emotionalter neural responses to amusing and sad films? NeuroImage, 27,656–668.

Iacoboni, M. (2005). Understanding others: Imitation, language, empa-thy. In S. Hurley, &N. Chater (Eds.), Perspectives on imitation: Fromcognitive neuroscience to social science: Vol. 1:Mechanisms of imitationand imitation in animals (pp. 77–99). Cambridge, MA: MIT Press.

Izard, C. E. (1991). The psychology of emotions. New York: Plenum.Keltner, D., Moffitt, T., & Stouthamer-Loeber, M. (1995). Facial

expressions of emotion and psychopathology in adolescent boys.Journal of Abnormal Psychology, 104, 644–652.

Kettunen, J., Ravaja, N., Naatanen, P., & Keltikangas-Jarvinen, L.(2000). The relationship of respiratory sinus arrhythmia to theco-activation of autonomic and facial responses during the Rorschachtest. Psychophysiology, 37, 242–250.

Knitzer, J., Steinberg, Z., & Fleisch, B. (1991). Schools, children’smentalhealth, and the advocacy challenge. Journal of Clinical Child Psy-chology, 20, 102–111.

Kring, A., Kerr, S., Smith, D., & Neale, J. (1993). Flat affect in schizo-phrenia does not reflect diminished subjective experience of emotion.Journal of Abnormal Psychology, 102, 507–517.

Lanzetta, J. T., Cartwright-Smith, J., & Kleck, R. E. (1976). Effects ofnonverbal dissimulation on emotional experience and autonomicarousal. Journal of Personality and Social Psychology, 33, 354–370.

Levenson, R. W. (1992). Autonomic nervous system differences amongemotions. Psychological Science, 3, 23–27.

Levenson, R. W. (1994). Human emotions: A functional view. In P.Ekman, &R. J. Davidson (Eds.), The nature of emotion: Fundamentalquestions (pp. 123–126). New York: Oxford University Press.

Levenson, R. W. (2003). Blood, sweat and fears: The autonomic archi-tecture of emotion. Annals of the New York Academy of Sciences,1000, 348–366.

Levenson, R. W., & Ruef, A. M. (1992). Empathy: A physiologicalsubstrate. Journal of Personality and Social Psychology, 63,234–246.

Liew, J., Eisenberg, N., Losoya, S. H., Fabes, R. A., Guthrie, I. K., &Murphy, B. C. (2003). Children’s physiological indices of empathyand their socioemotional adjustment: Does caregivers’ expressivitymatter? Journal of Family Psychology, 17, 584–597.

Lorber, M. F. (2004). Psychophysiology of aggression, psychopathy,and conduct problems: A meta-analysis. Psychological Bulletin, 130,531–552.

Mauss, I., Levenson, R., McCarter, L., Wilhelm, F., & Gross, J. J.(2005). The tie that binds? Coherence among emotion experience,behavior, and physiology. Emotion, 5, 175–190.

Mauss, I., Wilhelm, F. H., & Gross, J. J. (2004). Is there less to socialanxiety than meets the eye? Emotion experience, expression, andbodily responding. Cognition and Emotion, 18, 631–642.

Mezzacappa, E., Tremblay, R. E., Kindlon, D., Saul, J. P., Arseneault,L., & Seguin, J., et al. (1997). Anxiety, antisocial behavior, and heartrate regulation in adolescent males. Journal of Child Psychology andPsychiatry, 38, 457–469.

Niedenthal, P., Brauer, M., Halberstadt, J., & Innes-Ker, A. (2001).When did her smile drop? Facial mimicry and the influences of emo-tional state on the detection of change in emotional expression. Cog-nition and Emotion, 15, 853–864.

Notarius, C. I., & Levenson, R. W. (1979). Expressive tendencies andphysiological response to stress. Journal of Personality and SocialPsychology, 37, 1204–1210.

Ortiz, J., & Raine, A. (2004). Heart rate level and antisocial behavior inchildren and adolescents: A meta-analysis. Journal of the AmericanAcademy of Child & Adolescent Psychiatry, 43, 154–162.

Porges, S. W. (1995). Orienting in a defensive world: Mammalian mod-ifications of our evolutionary heritage. A polyvagal theory. Psycho-physiology, 32, 301–318.

Porges, S.W. (1997). Emotion: An evolutionary by-product of the neuralregulation of the autonomic nervous system. Annals of the New YorkAcademy of Sciences, 807, 62–77.

Porges, S. W. (2001). The polyvagal theory: Phylogenetic substrates of asocial nervous system. International Journal of Psychophysiology, 42,123–146.

Porges, S. W. (2007). The polyvagal perspective. Biological Psychology,74, 116–143.

Qu, M., Zhang, Y., Webster, J. G., & Tompkins, W. J. (1986). Motionartifact from spot and band electrodes during impedance cardiogra-phy. Transactions on Biomedical Engineering, 11, 1029–1036.

Raudenbush, S., Bryk, A., Cheong, Y. F., & Congdon, R. (2004).HLM6: Hierarchical linear and nonlinear modeling. Lincolnwood, IL:Scientific Software International.

Rogosa, D., Brandt, D., & Zimowski, M. (1982). A growth curveapproach to the measurement of change. Psychological Bulletin, 92,726–748.

Rottenberg, J., Kasch, K. L., Gross, J. J., &Gotlib, I. H. (2002). Sadnessand amusement reactivity differentially predict concurrent andprospective functioning in major depressive disorder. Emotion, 2,135–146.

Rottenberg, J., Salomon, K., Gross, J. J., & Gotlib, I. H. (2005). Vagalwithdrawal to a sad film predicts recovery from depression. Psycho-physiology, 42, 277–281.

Sherwood, A., Allen, M. T., Fahrenberg, J., Kelsey, R. M., Lovallo, W.R., & van Doornen, L. J. (1990). Methodological guidelines for im-pedance cardiography. Psychophysiology, 27, 1–23.

Sherwood, A., Allen, M. T., Obrist, P. A., & Langer, A. W. (1986).Evaluation of beta-adrenergic influences on cardiovascular and met-abolic adjustments to physical and psychological stress. Psychophys-iology, 23, 89–104.

Sloan, D. M., Strauss, M. E., Quirk, S. W., & Sajatovic, M. (1997).Subjective and expressive emotional response in depression. Journalof Affective Disorders, 46, 135–141.

Speer, D. C., & Greenbaum, P. E. (1995). Five methods for computingindividual client change and improvement rates: Support for an in-dividual growth curve approach. Journal of Consulting and ClinicalPsychology, 63, 1044–1048.

Sponheim, S. R., Allen, J. J., & Iacono, W. G. (1995). Selected psycho-physoiological measures in depression: The significance of electrode-rmal activity, electroencephalographic asymmetries, and contingentnegative variation to behavioral and neurobiological aspects ofdepression. In G. A.Miller (Ed.), The behavioral high risk paradigm inpsychopathology (pp. 222–249). New York: Springer.

Stevens, D., Charman, T., & Blair, R. J. R. (2001). Recognition of emo-tion in facial expressions and vocal tones in children with psycho-pathic tendencies. Journal of Genetic Psychology, 162, 201–211.

Strand, K., & Nowicki, S. (1999). Receptive nonverbal processing abilityand locus of control orientation in children and adolescents withconduct disorder. Behavioral Disorders, 24, 102–108.

Thayer, J. F., Friedman, B. H., & Borkovec, T. D. (1996). Autonomiccharacteristics of generalized anxiety and worry. Biological Psychia-try, 39, 255–266.

Tsai, J. L., Levenson, R. W., & Carstensen, L. (2000). Autonomic, sub-jective, and expressive responses to emotional films in older andyounger Chinese Americans and European Americans. Psychologyand Aging, 15, 684–693.

Walbott, H. G. (1991). Recognition of emotion from facial expression viaimitation? Some indirect evidence for an old theory. British Journal ofSocial Psychology, 30, 207–219.

Zahn-Waxler, C., Cole, P. M., Welsh, J. D., & Fox, N. A. (1995).Psychophysiological correlates of empathy and prosocial behaviorsin preschool children with behavior problems. Development andPsychopathology, 7, 27–48.

(Received May 27, 2006; Accepted July 15, 2007)

110 P. Marsh, T.P. Beauchaine, and B. Williams